Heme oxygenase 2 deficiency increases brain swelling and inflammation after intracerebral hemorrhage

Neuroscience

Volumn 155, Issue 4, 2008, Pages 1133-1141

  Wang, J ^a   Dore S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

astrocytes; blood; brain edema; hemispheric enlargement; reactive oxygen species; stroke

Indexed keywords

COLLAGENASE; CYTOCHROME C; HEME OXYGENASE 2; PEROXYNITRITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOMA; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN WATER; CELL ACTIVATION; CONTROLLED STUDY; DNA DAMAGE; ENCEPHALITIS; ENZYME DEFICIENCY; IMMUNOCOMPETENT CELL; KNOCKOUT MOUSE; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; WATER CONTENT;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN EDEMA; CALCIUM-BINDING PROTEINS; CEREBRAL HEMORRHAGE; CYTOCHROMES C; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR, RECOMBINANT; HEME OXYGENASE (DECYCLIZING); INTERLEUKIN-3; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; ORGANIC CHEMICALS; RECOMBINANT FUSION PROTEINS; SPECTROPHOTOMETRY; TIME FACTORS; TYROSINE;

EID: 50249135422     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.07.004     Document Type: Article

References (43)

1. Anderson M.F., Blomstrand F., Blomstrand C., Eriksson P.S., and Nilsson M. Astrocytes and stroke: networking for survival?. Neurochem Res 28 (2003) 293-305
2. Aronowski J., and Hall C.E. New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res 27 (2005) 268-279
3. Chang E.F., Wong R.J., Vreman H.J., Igarashi T., Galo E., Sharp F.R., Stevenson D.K., and Noble-Haeusslein L.J. Heme oxygenase-2 protects against lipid peroxidation-mediated cell loss and impaired motor recovery after traumatic brain injury. J Neurosci 23 (2003) 3689-3696
4. Clark W., Gunion-Rinker L., Lessov N., and Hazel K. Citicoline treatment for experimental intracerebral hemorrhage in mice. Stroke 29 (1998) 2136-2140
5. Del Bigio M.R., Yan H.J., Buist R., and Peeling J. Experimental intracerebral hemorrhage in rats. Magnetic resonance imaging and histopathological correlates. Stroke 27 (1996) 2312-2319 discussion 2319-2320
6. Doré S. Decreased activity of the antioxidant heme oxygenase enzyme: implications in ischemia and in Alzheimer's disease. Free Radic Biol Med 32 (2002) 1276-1282
7. Doré S., Goto S., Sampei K., Blackshaw S., Hester L.D., Ingi T., Sawa A., Traystman R.J., Koehler R.C., and Snyder S.H. Heme oxygenase-2 acts to prevent neuronal death in brain cultures and following transient cerebral ischemia. Neuroscience 99 (2000) 587-592
8. Doré S., Sampei K., Goto S., Alkayed N.J., Guastella D., Blackshaw S., Gallagher M., Traystman R.J., Hurn P.D., Koehler R.C., and Snyder S.H. Heme oxygenase-2 is neuroprotective in cerebral ischemia. Mol Med 5 (1999) 656-663
9. Eder C. Regulation of microglial behavior by ion channel activity. J Neurosci Res 81 (2005) 314-321
10. Facchinetti F., Dawson V.L., and Dawson T.M. Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18 (1998) 667-682
11. Garrido C., Galluzzi L., Brunet M., Puig P.E., Didelot C., and Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13 (2006) 1423-1433
12. Geisler S., Heilmann H., and Veh R.W. An optimized method for simultaneous demonstration of neurons and myelinated fiber tracts for delineation of individual trunco- and palliothalamic nuclei in the mammalian brain. Histochem Cell Biol 117 (2002) 69-79
13. Ito D., Tanaka K., Suzuki S., Dembo T., and Fukuuchi Y. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32 (2001) 1208-1215
14. Kondo T., Reaume A.G., Huang T.T., Carlson E., Murakami K., Chen S.F., Hoffman E.K., Scott R.W., Epstein C.J., and Chan P.H. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17 (1997) 4180-4189
15. MacLellan C.L., and Colbourne F. Mild to moderate hyperthermia does not worsen outcome after severe intracerebral hemorrhage in rats. J Cereb Blood Flow Metab 25 (2005) 1020-1029
16. Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A.W., Chan P., and Verkman A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6 (2000) 159-163
17. Marla S.S., Lee J., and Groves J.T. Peroxynitrite rapidly permeates phospholipid membranes. Proc Natl Acad Sci U S A 94 (1997) 14243-14248
18. Matsushita K., Meng W., Wang X., Asahi M., Asahi K., Moskowitz M.A., and Lo E.H. Evidence for apoptosis after intercerebral hemorrhage in rat striatum. J Cereb Blood Flow Metab 20 (2000) 396-404
19. Matz P.G., Fujimura M., Lewen A., Morita-Fujimura Y., and Chan P.H. Increased cytochrome c-mediated DNA fragmentation and cell death in manganese-superoxide dismutase-deficient mice after exposure to subarachnoid hemolysate. Stroke 32 (2001) 506-515
20. Miller G. Neuroscience. The dark side of glia. Science 308 (2005) 778-781
21. Poss K.D., and Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 94 (1997) 10919-10924
22. Qu Y., Chen-Roetling J., Benvenisti-Zarom L., and Regan R.F. Attenuation of oxidative injury after induction of experimental intracerebral hemorrhage in heme oxygenase-2 knockout mice. J Neurosurg 106 (2007) 428-435
23. Qureshi A.I., Suri M.F., Ostrow P.T., Kim S.H., Ali Z., Shatla A.A., Guterman L.R., and Hopkins L.N. Apoptosis as a form of cell death in intracerebral hemorrhage. Neurosurgery 52 (2003) 1041-1047 discussion 1047-1048
24. Rogers B., Yakopson V., Teng Z.P., Guo Y., and Regan R.F. Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Radic Biol Med 35 (2003) 872-881
25. Rogove A.D., Lu W., and Tsirka S.E. Microglial activation and recruitment, but not proliferation, suffice to mediate neurodegeneration. Cell Death Differ 9 (2002) 801-806
26. Rosenberg G.A., Mun-Bryce S., Wesley M., and Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke 21 (1990) 801-807
27. Schmued L.C., and Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874 (2000) 123-130
28. Smith A. Homeostasis of heme in health and disease: current aspects of the structural biology of heme-protein interactions and of gene regulation. DNA Cell Biol 21 (2002) 245-249
29. Tang J., Liu J., Zhou C., Alexander J.S., Nanda A., Granger D.N., and Zhang J.H. MMP-9 deficiency enhances collagenase-induced intracerebral hemorrhage and brain injury in mutant mice. J Cereb Blood Flow Metab 24 (2004) 1133-1145
30. Tejima E., Zhao B.Q., Tsuji K., Rosell A., van Leyen K., Gonzalez R.G., Montaner J., Wang X., and Lo E.H. Astrocytic induction of matrix metalloproteinase-9 and edema in brain hemorrhage. J Cereb Blood Flow Metab 27 (2007) 460-468
31. Wagener F.A.D.T.G., Eggert A., Boerman O.C., Oyen W.J.G., Verhofstad A., Abraham N.G., Adema G., van Kooyk Y., de Witte T., and Figdor C.G. Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood 98 (2001) 1802-1811
32. Wang J., and Doré S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 130 (2007) 1643-1652
33. Wang J., and Doré S. Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab 27 (2007) 894-908
34. Wang J., Fields J., Zhao C., Langer J., Thimmulappa R.K., Kensler T.W., Yamamoto M., Biswal S., and Doré S. Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med 43 (2007) 408-414
35. Wang J., Rogove A.D., Tsirka A.E., and Tsirka S.E. Protective role of tuftsin fragment 1-3 in an animal model of intracerebral hemorrhage. Ann Neurol 54 (2003) 655-664
36. Wang J., and Tsirka S.E. Contribution of extracellular proteolysis and microglia to intracerebral hemorrhage. Neurocrit Care 3 (2005) 77-85
37. Wang J., and Tsirka S.E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 128 (2005) 1622-1633
38. Wang J., Zhuang H., and Doré S. Heme oxygenase 2 is neuroprotective against intracerebral hemorrhage. Neurobiol Dis 22 (2006) 473-476
39. Wasserman J.K., and Schlichter L.C. Minocycline protects the blood-brain barrier and reduces edema following intracerebral hemorrhage in the rat. Exp Neurol 207 (2007) 227-237
40. Wasserman J.K., and Schlichter L.C. Neuron death and inflammation in a rat model of intracerebral hemorrhage: effects of delayed minocycline treatment. Brain Res 1136 (2007) 208-218
41. Weiss S.J. Tissue destruction by neutrophils. N Engl J Med 320 (1989) 365-376
42. Xi G., Keep R.F., and Hoff J.T. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5 (2006) 53-63
43. Xue M., Hollenberg M.D., and Yong V.W. Combination of thrombin and matrix metalloproteinase-9 exacerbates neurotoxicity in cell culture and intracerebral hemorrhage in mice. J Neurosci 26 (2006) 10281-10291